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Impact of gut microbiota on the fly's germ line.

Elgart M, Stern S, Salton O, Gnainsky Y, Heifetz Y, Soen Y - Nat Commun (2016)

Bottom Line: Unlike vertically transmitted endosymbionts, which have broad effects on their host's germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line.We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies.The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry, Weizmann Institute of Science, Rehovot 76100, Israel.

ABSTRACT
Unlike vertically transmitted endosymbionts, which have broad effects on their host's germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line. Here we provide evidence supporting the influence of these gut bacteria on the germ line of Drosophila melanogaster. Removal of the gut bacteria represses oogenesis, expedites maternal-to-zygotic-transition in the offspring and unmasks hidden phenotypic variation in mutants. We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies. The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.

No MeSH data available.


Related in: MedlinePlus

Removal of extracellular gut bacteria exposes 'hidden' mutations and reduces stress tolerance in the next generation.(a) Effect of removal of gut bacteria in F1 on the kinetics of pupation in F1 and F2, shown for wild-type flies (yw) and 4 mutant lines (InR, trx, pcl and Aldh). Inset: statistical analysis of the variance in pupation time due to difference in genotype. Shown are variances in genotype-specific median time to pupation. Mean variance±s.e., n=3. Note the substantially larger variance in F2 versus F1. ***P<0.001 (Student's t-test). (b) Effect of removal of gut bacteria in F1 on the survival of F2 drm>neoGFP flies that were exposed to 400 μg ml−1 of G418 in both generations. Note the strong reduction in the survival of F2 flies when G418 treatment was preceded by egg dechorionation in F1. Mean survival to adulthood relative to untreated control±s.e., n=3, **P<0.01 (Student's t-test).
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f4: Removal of extracellular gut bacteria exposes 'hidden' mutations and reduces stress tolerance in the next generation.(a) Effect of removal of gut bacteria in F1 on the kinetics of pupation in F1 and F2, shown for wild-type flies (yw) and 4 mutant lines (InR, trx, pcl and Aldh). Inset: statistical analysis of the variance in pupation time due to difference in genotype. Shown are variances in genotype-specific median time to pupation. Mean variance±s.e., n=3. Note the substantially larger variance in F2 versus F1. ***P<0.001 (Student's t-test). (b) Effect of removal of gut bacteria in F1 on the survival of F2 drm>neoGFP flies that were exposed to 400 μg ml−1 of G418 in both generations. Note the strong reduction in the survival of F2 flies when G418 treatment was preceded by egg dechorionation in F1. Mean survival to adulthood relative to untreated control±s.e., n=3, **P<0.01 (Student's t-test).

Mentions: The above analysis was performed in wild-type flies under conditions which promote robust propagation of lab strains and might therefore mask some of the impacts of bacterial depletion. We therefore evaluated functional consequences of removing bacteria on the background of genetic changes and environmental stress. In particular, we tested if loss of gut bacteria influences phenotypic stability in several fly lines carrying heterozygous mutations in the following genes: polycomb-like (pcl), trithorax (trx), insulin receptor (InR) and Aldh (not a line). We removed gut bacteria by egg dechorionation and analysed the rate of pupation in the same generation (F1) and the following generation (F2). While none of the mutations influenced the rate of pupation in F1, they led to substantial, mutation-specific differences in the offspring generation (Fig. 4a). Thus, the lack of gut bacteria uncovered mutation-specific phenotypes in F2 that were masked in F1. The unmasking of mutations only in the second generation suggests that the removal of bacteria in F1 destabilizes embryogenesis in F2 to an extent that no longer supports phenotypic buffering of the mutations. To test if such destabilization can also affect stress tolerance without mutations, we used the toxicity model of Stern et al.43. Specifically, we generated transgenic drm>neoGFP flies carrying a G418-resistance gene (neoGFP) under the control of the drumstick (drm) promoter and investigated G418 tolerance in F2 larvae with and without prior removal of gut bacteria by egg dechorionation in F1. The pre-elimination of gut bacteria in F1 led to much stronger reduction in the survival of F2 offspring that were exposed to G418 in both generations (Fig. 4b). This differential stress tolerance suggests that removal of bacteria destabilizes subsequent embryogenesis to an extent which severely compromises resistance to toxic stress in F2.


Impact of gut microbiota on the fly's germ line.

Elgart M, Stern S, Salton O, Gnainsky Y, Heifetz Y, Soen Y - Nat Commun (2016)

Removal of extracellular gut bacteria exposes 'hidden' mutations and reduces stress tolerance in the next generation.(a) Effect of removal of gut bacteria in F1 on the kinetics of pupation in F1 and F2, shown for wild-type flies (yw) and 4 mutant lines (InR, trx, pcl and Aldh). Inset: statistical analysis of the variance in pupation time due to difference in genotype. Shown are variances in genotype-specific median time to pupation. Mean variance±s.e., n=3. Note the substantially larger variance in F2 versus F1. ***P<0.001 (Student's t-test). (b) Effect of removal of gut bacteria in F1 on the survival of F2 drm>neoGFP flies that were exposed to 400 μg ml−1 of G418 in both generations. Note the strong reduction in the survival of F2 flies when G418 treatment was preceded by egg dechorionation in F1. Mean survival to adulthood relative to untreated control±s.e., n=3, **P<0.01 (Student's t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835552&req=5

f4: Removal of extracellular gut bacteria exposes 'hidden' mutations and reduces stress tolerance in the next generation.(a) Effect of removal of gut bacteria in F1 on the kinetics of pupation in F1 and F2, shown for wild-type flies (yw) and 4 mutant lines (InR, trx, pcl and Aldh). Inset: statistical analysis of the variance in pupation time due to difference in genotype. Shown are variances in genotype-specific median time to pupation. Mean variance±s.e., n=3. Note the substantially larger variance in F2 versus F1. ***P<0.001 (Student's t-test). (b) Effect of removal of gut bacteria in F1 on the survival of F2 drm>neoGFP flies that were exposed to 400 μg ml−1 of G418 in both generations. Note the strong reduction in the survival of F2 flies when G418 treatment was preceded by egg dechorionation in F1. Mean survival to adulthood relative to untreated control±s.e., n=3, **P<0.01 (Student's t-test).
Mentions: The above analysis was performed in wild-type flies under conditions which promote robust propagation of lab strains and might therefore mask some of the impacts of bacterial depletion. We therefore evaluated functional consequences of removing bacteria on the background of genetic changes and environmental stress. In particular, we tested if loss of gut bacteria influences phenotypic stability in several fly lines carrying heterozygous mutations in the following genes: polycomb-like (pcl), trithorax (trx), insulin receptor (InR) and Aldh (not a line). We removed gut bacteria by egg dechorionation and analysed the rate of pupation in the same generation (F1) and the following generation (F2). While none of the mutations influenced the rate of pupation in F1, they led to substantial, mutation-specific differences in the offspring generation (Fig. 4a). Thus, the lack of gut bacteria uncovered mutation-specific phenotypes in F2 that were masked in F1. The unmasking of mutations only in the second generation suggests that the removal of bacteria in F1 destabilizes embryogenesis in F2 to an extent that no longer supports phenotypic buffering of the mutations. To test if such destabilization can also affect stress tolerance without mutations, we used the toxicity model of Stern et al.43. Specifically, we generated transgenic drm>neoGFP flies carrying a G418-resistance gene (neoGFP) under the control of the drumstick (drm) promoter and investigated G418 tolerance in F2 larvae with and without prior removal of gut bacteria by egg dechorionation in F1. The pre-elimination of gut bacteria in F1 led to much stronger reduction in the survival of F2 offspring that were exposed to G418 in both generations (Fig. 4b). This differential stress tolerance suggests that removal of bacteria destabilizes subsequent embryogenesis to an extent which severely compromises resistance to toxic stress in F2.

Bottom Line: Unlike vertically transmitted endosymbionts, which have broad effects on their host's germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line.We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies.The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry, Weizmann Institute of Science, Rehovot 76100, Israel.

ABSTRACT
Unlike vertically transmitted endosymbionts, which have broad effects on their host's germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line. Here we provide evidence supporting the influence of these gut bacteria on the germ line of Drosophila melanogaster. Removal of the gut bacteria represses oogenesis, expedites maternal-to-zygotic-transition in the offspring and unmasks hidden phenotypic variation in mutants. We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies. The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.

No MeSH data available.


Related in: MedlinePlus